Biogeography and taxonomy of New Zealand Cladocera (Anomopoda, Chydoridae): a review

Abstract

Studies of the biogeography of Cladocera in New Zealand lakes are rare and only a few species of littoral chydorid Cladocera have been documented. Consequently, a number of issues relating to their taxonomy and systematics have yet to be resolved. The majority of chydorid Cladocera in the northern hemisphere have been given new names after a detailed investigation of their morphology and genetic variability. However, knowledge of their inter-hemispheric distribution is poor. It is likely that many species of chydorid Cladocera in the southern hemisphere, including in the New Zealand lakes, will show significant genetic variability from their northern hemisphere counterparts, although this has not yet been investigated. Here we review the taxonomy and biogeography of the New Zealand chydorid Cladocera. This is important when we consider the limited knowledge of New Zealand cladocerans and the consequent difficulties encountered by freshwater ecologists and paleolimnologists when using them to identify rapid environmental changes in the southern hemisphere.

Keywords:

• biogeography
• taxonomy
• chydorid Cladocera
• New Zealand

Introduction

New Zealand has an extensive network of freshwater systems comprising streams, braided and meandering rivers, mountain and lowland lakes and a wide range of wetland complexes across the coastal margins that embodies a unique ecosystem and biodiversity in the southern hemisphere. However, compared to their terrestrial counterparts, freshwater ecosystems in New Zealand have been relatively under-studied, with the focus on vertebrate fish to date (McDowall 1990). The macro- and micro-invertebrates, including the cladocerans, have received a very little attention so the biogeography and taxonomy of these organisms are poorly understood in New Zealand. The poor state of cladoceran taxonomy in New Zealand has made it difficult to apply them to understanding lacustrine ecosystems and the records of global environmental change they contain.

Chydorids are a distinct group of organisms within the family Chydoridae. They span a wide range of habitats including littoral mud, submerged vegetation, sandy substrata and open lake environments (Smirnov 1971; Whiteside 1974). They feed at the substrate–water interface where they obtain food by scraping algae and detritus from surfaces over which they crawl or from sediments in which they burrow (Fryer 1974; Frey 1976; Whiteside & Swindoll 1988). Many taxa within the family Chydoridae are important indicators for temperature, lake water pH and nutrient dynamics (Whiteside & Swindoll 1988). The taxa differ greatly with seasons and habitat types (Whiteside 1974; Whiteside et al. 1978). Taxa such as Graptoleberis testudinaria Fischer, 1848 and Alona affinis Leydig, 1860 prefer plant macrophytes submerged, while other taxon such as Monospilus dispar Sars, 1862 prefers sandy substrata (Dole-Olivier et al. 2000).

A strong response of chydorid assemblages to environmental gradients such as surface water temperatures and total phosphorus (TP) in European mountain lakes was reported by Lotter et al. (1997). In Europe, relatively warm-climate-preferring taxa belonging to small Alona groups (e.g. Alona guttata Sars, 1862) were predominantly recorded from the low-altitude temperate regions (Korhola 1999), while the cold-climate-preferring taxa such as Acroperus harpae Baird, 1836 and Alona affinis Leydig, 1860 predominantly occurred in sub-arctic and high-altitude sites (Hofmann 2000). Temperature also plays a profound role in the life history of these cladocerans (Nevalainen & Luoto 2010). Adult females produce a large number of parthenogenetic females during spring (Frey 1982a). However, under adverse climatic conditions (e.g. a dry period) gamogenesis occurs when females produce haploid reproductive or resting eggs (Frey 1982a).

Recently, species-specific temperature optima and the tolerance range of chydorid Cladocera has been investigated in Europe for control of gamogenesis. Using a weighted averaging (WA) approach, Alonella excisa Fischer, 1854 and Graptoleberis testudinaria Fisher, 1848 showed increased temperature optima ranges compared with Alonella nana Baird, 1850 and Chydorus sphaericus Müller, 1776 for gamogenesis (Nevalainen & Luoto 2010). Depending on climate, weather conditions and topography such as mountains, drylands and wetlands the resting eggs are transported widely via rivers, lake systems and even by birds, mammals and insects and by wind (Maguire 1963; Figuerola & Green 2002). Consequently, those species which were able to adapt the new environment over million years may have established their populations widely across hemispheres.

Until recently, the New Zealand chydorid Cladocera had been considered to be ubiquitous species based on their morphological resemblance to their northern hemisphere counterparts (Frey 1982b ,1987). However, Korovchinsky (2006) argued that most chydorid Cladocera described previously from New Zealand lakes should not be considered as cosmopolitan species. As a result of confusion that exists in the taxonomy and biogeography of these organisms, the use of chydorid cladocerans as proxy indicators of change in New Zealand lakes has faced difficulties.

The geological history of New Zealand could have played a major role in speciation of chydorid Cladocera, thereby reducing the cosmopolitanism. The influence of continental break-up, creation of oceanic barriers for transport of resting eggs as well as rapid tectonic movements in the region should have been the major factors in evolution of cladocerans in New Zealand and the increased tendency to endemism due to speciation (Frey 1995).

At present, only 40–45% of cladoceran species are identified confidently, as taxonomic issues have yet to be resolved with the family Chydoridae (Forrò et al. 2008). Several revisions to the taxonomy and systematics of the chydorid Cladocera have been made (Frey 1987; Korovchinsky 1996 ,1997; Kotov 2009) based on analyses of both modern (Sinev 2004) and fossil (Frey 1987) cladoceran morphological variability in body parts and ontogenic change (Sacherova & Hebert 2003). However, pertinent taxonomic studies in New Zealand lakes are few. The present review will contribute to our understanding of the status of the taxonomy and biogeography of the chydorid Cladocera in New Zealand. This information is crucial for their application to studies of local and regional environmental change over varying time scales.

Methods of collecting intact and fossil chydorid Cladocera

Modern and fossil chydorid Cladocera need to be collected from lakes and reservoirs using a variety of methods for biogeographical and taxonomic investigations. Whiteside (1974) used Tuffy balls (plastic mesh balls) manufactured for scrubbing dishes and placed them in submerged vegetation. Once the balls were sufficiently colonized by algae and bacteria (ca 5 days), a wide range of chydorid species used these balls as their food-habitats. Hann (1995) used a downing box sampler, a rigid plastic enclosure, for sampling these biota. The organisms were collected by lowering the sampler into the water and cutting the stems of macrophytes containing the chydorids. Funnel-shaped nets or sweep nets and pattern samplers, usually with 100 µm size, have also been used frequently for sampling littoral chydorids (e.g. Whiteside 1974; Kattel et al. 2006; Nevalainen & Luoto 2010).

The taxonomy of recent and ancient chydorid cladocerans improved significantly once the remains of cladocerans in lake sediment surface and core samples began to be analysed (Frey 1960a). Surface and long sediment cores are collected using a variety of techniques. A simple gravity-operated sampling device has been commonly used for recovery of lacustrine sediments (Glew & Last 2001). Following the subsampling of the sediment core, a few grams (ca 1–3 g) of sediments are treated with 10% KOH solution with ca 200 mL water. The solution is placed on a hotplate at 60°C for at least three-quarters of an hour. The treated sample is then cleaned thoroughly before being prepared for a high-resolution slide for taxonomic analysis. The chydorid body parts such as head shield, post abdomen, carapace, ephippium and post-abdominal claws are then examined under a microscope at 100× and 400× magnification. Based on morphological characters of the body parts, the taxonomy of chydorids is identified (Frey 1986; Korhola & Rautio 2001; Kattel & Augustinus 2010).

However, recently, DNA analysis of chydorid Cladocera has become more important since the accuracy of the taxonomy of these animals has increased significantly using these analyses (Sacherova & Hebert 2003). These molecular studies suggest that there should be two to four times more cladoceran species than currently documented worldwide (Adamowicz & Purvis 2005; Forró et al. 2008) and the New Zealand chydorid Cladocera should be no exception to this.

Global status of the biogeography and taxonomy of chydorid Cladocera

The chydorid Cladocera were first described by OF Müller in 1769. He focused mainly on chydorid genera such as Eurycercus, Camptocercus, Alona, Pleuroxus and Chydorus (Müller 1785). Over the next hundred years or so, study of the taxonomy of the chydorid Cladocera was confined to Europe, where the systematics of most genera became well established (Frey 1995). In the later part of the nineteenth century, the taxonomic focus shifted to species level in both Europe and overseas. In the 1860s, GO Sars described more than 16 species of chydorid Cladocera from Norway only (Sars 1993). Later, Birge (1918) described several chydorid species from different parts of the world including North America, South America, Sri Lanka and Australia. Although the taxonomic study of the chydorid Cladocera was extended globally, most species recorded outside Europe were described as though they were European species. A significant breakthrough in examination of differences in genera and species of the chydorid cladoceran extant between Europe and other continents occurred only in the later part of the twentieth century. DG Frey and NN Smirnov made significant contributions in this regard; for example, their clarification of the confusion between the genus Eurycercus in Europe and Sayca in Australia and New Zealand (Frey 1971). The interhemispheric taxonomic variation of genera Chydorus, Pleuroxus and Ephemeroporus has also been updated (Frey 1982b; Smirnov 2007) and species within the genus Alona have been comprehensively described (Sinev 2004; Van Damme et al. 2010). Nevertheless, understanding of the taxonomy and systematics of New Zealand chydorid Cladocera is still poor.

Biogeography and taxonomy of New Zealand chydorid Cladocera

Until recently, the New Zealand chydorid Cladocera were little documented due to use of the northern hemisphere taxonomy. Hence the taxonomy and systematics of most species of New Zealand chydorid Cladocera require a comprehensive review to be able to assess the number of endemic species in New Zealand lakes. The majority of studies of New Zealand lake biota have focused on general distribution patterns of zooplankton groups (e.g. cladocerans, copepods, rotifers, etc.) (Forsyth & McCallum 1980; Greenwood et al. 1999; Hall & Burns 2003) or genera (e.g. Bosmina, Ceriodaphnia, Daphnia, Alona, Chydorus, etc.) (Chapman & Green 1999; Burger et al. 2002; Schallenberg et al. 2003) across the seasons and habitat types, and trophic interactions such as fish vs zooplankton (Jeppesen et al. 1997 ,2000), or zooplankton vs phytoplankton (James & Forsyth 1990). However, comprehensive study of chydorid cladocerans is lacking, including well-defined taxonomy to species level and their temporal and spatial distribution patterns. The records of chydorid cladocerans identified to species level are crucial for understanding species-specific preferences for structural habitats, their geographical distribution as well as species optima and tolerance to a variety of physicochemical variables (e.g. temperature, TP, salinity) in New Zealand lakes (Fig. 1). DG Frey studied the biogeography and taxonomy of the New Zealand chydorid Cladocera based on their remains in sediment from North Island lakes (Frey 1991a). Significant morphological variability was encountered such as differences in body size, head pores and postabdominal teeth from their northern hemisphere counterparts and argued for the presence of increasingly endemic species adapted for New Zealand climates (Frey 1971 ,1991a).

Fig. 1  Map illustrating the locations of previously studied sites of cladoceran zooplankton in New Zealand lake and river systems. (a) Lake Oneopoto (paleolake) North Island (Kattel & Augustinus 2010); (b) Lake Ohau and Tekapo South Island (Burns et al. 1984).

There are eight species of endemic chydorid Cladocera in New Zealand lakes (Chapman & Lewis 1976; Frey 1995). Australian lakes have a far higher number of endemic species (N=41) (Smirnov & Timms 1983; Frey 1991a ,1995). However, there are many similarities between the chydorid Cladocera present in Australia and New Zealand. For example, the polyembroynic genus Saycia occurs only in Australia and New Zealand, and the genus Pleuroxus are also abundant in Australia and New Zealand lakes (Frey 1993a ,b; Shiel & Dickson 1995).

Variability in morphology of some species of chydorid Cladocera between New Zealand and Australia has also been reported. The New Zealand species of Saycia, Saycia cooki novaezealandie Frey, 1971, has been shown to be different from its Australian counterpart, Saycia cooki cooki King, 1866 (Table 1). S. cooki novaezealandie have more preanal teeth on the post-abdomen and have a shorter posterior margin relative to the length of the animal (Frey 1971).

Table 1  List of New Zealand (as well as southern Australia and Tasmania) chydorid Cladocera reported in various literature.

Subfamily	Species	Distribution	Comments	Reference
Sayciinae	Sacia cooki novaezealandie Frey, 1971	New Zealand	endemic	Frey 1971
Chydorinae	Alonella excisa Fischer, 1854	Australia, New Zealand	cosmopolitan	Shiel &Dickson 1995, Kattel & Augustinus 2010
	A. nana Baird, 1850	New Zealand*	cosmopolitan	Kattel & Augustinus 2010
	Ephemeroporus barroisi Richard, 1894	New Zealand	endemic	Burns et al. 1984
	Dunhevedia crassa King, 1853	Australia, New Zealand	cosmopolitan	Frey 1991a, Shiel & Dickson 1995
	Pleuroxus hastirostris Sars, 1904	New Zealand	endemic	Smirnov & Timms 1983, Frey 1993
	P. helvencus Frey 1991	New Zealand	endemic	Smirnov & Timms 1983, Frey 1993
	Pseudochydorus globosus Baird, 1843	Australia, New Zealand	cosmopolitan	Frey 1995
	Chydorus sphaericus Müller, 1776	Australia, New Zealand	cosmopolitan	Shiel & Dickson 1995, Kattel & Augustinus 2010
	C. minutus Thomson, 1978	New Zealand	endemic	Frey 1993
Aloninae	Camptocercus australis Sars, 1896	Australia, New Zealand	endemic	Byars 1959, Shiel & Dickson 1995, Smirnov 1998
	Oxyurella tenuicaudis Sars, 1862	Australia, New Zealand	cosmopolitan	Shiel & Dickson 1995
	Leydigia leydigi Schoedler, 1863	Australia, New Zealand	cosmopolitan	Shiel & Dickson 1995
	Alona setigera Brehm, 1931	Australia, New Zealand	cosmopolitan	Smirnov & Timms 1983
	A.guttata Sars, 1862	Australia, New Zealand	cosmopolitan	Smirnov & Timms 1983, Kattel & Augustinus 2010
	Armatalona macrocopa Smirnov, 1989	Australia, New Zealand	cosmopolitan	Smirnov 1989
	Biapertura affinis Leydig, 1860	Australia, New Zealand	cosmopolitan	Shiel & Dickson, Burger et al. 2002
	Bryospilus bifidus Frey, 1980	New Zealand	endemic	Frey 1980
	Graptoleberis testudinaria Fischer, 1848	Australia, New Zealand	cosmopolitan	Shiel & Dickson 1995, Kattel & Augustinus 2010
	Monospilus dispar Sars, 1862	New Zealand	cosmopolitan	Alonso 1996
For Australian chydorid cladocerans please refer to Shiel & Dickson (1995) in detail. Alonella excisa and Chydorus sphaericus recorded in various published literature in New Zealand lakes may be incorrectly identified. These cladocerans may be endemic species to New Zealand and should be redefined. Ephemeroporus barroisi also needs further clarification if this species is an endemic to New Zealand.
*Alonella nana was not documented from New Zealand lakes previously. Based on morphological features of head shield, head pores and post-abdomen, Kattel &Augustinus (2010) have reported the presence of A. nana in the Onepoto maar, Auckland. However, this needs to be verified.

The extended latitudinal variation of New Zealand lakes between North and South Islands further suggests that several species of New Zealand chydorid Cladocera may be endemic. Latitudinal influence on speciation of New Zealand chydorid Cladocera has not been documented. However, given the separation of North and South Islands as well as extreme climatic variation between far north (sub-tropical) and far south (sub-antarctic), speciation within the genera between two islands can also be a part of future investigations as Frey (1971) reported differences in the endemic species of the genus Saciya between Australia and New Zealand.

Some species-rich genera, e.g. Pleuroxus, Chydorus, Alona and Biapertura, have an inter-hemispheric distribution, with Chydorus dominant in North America and Biapertura dominant in Australia and New Zealand (Frey 1995). Studies of modern chydorid Cladocera in New Zealand lakes by Davids et al. (1987) and Burger et al. (2002) documented relatively wide distribution of Biapertura affinis Leydig, 1860. The use of genus Biapertura is different with respect to location of their collection. For example, a similar species has been documented as Biapertura macrocopa in Australia (Sinev 2004). From a maar lake in Auckland, New Zealand, Kattel & Augustinus (2010) reported large Alona-like species with a resemblance to the northern hemisphere species Alona affinis Leydig, 1860. However, it is possible that this specimen belongs to the Biapertura group of the southern hemisphere. Headshields of large Alona have been recorded from surface sediment samples from a lowland lake L0424 in the South Island of New Zealand (Fig. 2a).

Fig. 2  Headshields of some chydorid Cladocera recorded by GRK from the surface sediment samples of various lakes from South Island, New Zealand. Specimens are yet to be identified fully. (a) Lake L0424 (lowland grassland); (b) Lake L0407 (lowland forest); (c) Lake L0405 (lowland forest); (d) Lake L0412 (upland grassland); (e) Lake L0423 (lowland shrubland); (f) Lake L0419 (rocky catchment). Please refer to the text for details.

The headshields contained in the core sediment sample from the Auckland maar and the surface sediment samples from the South Island lake are significantly different with respect to the number of headpores. Unlike the headpores of Alona (Biapertura) affinis Leydig, 1860 (Sinev 1997), the Alona headshield from the South Island lake sediment has one median pore and two lateral pores connecting with a curve-like structure (Fig. 2a). Confirmation of the correct identification of large Alona including Alona affinis Leydig, 1860 and Biapertura affinis Leydig, 1860 through DNA analysis is required. Sacherova & Hebert (2003) also showed that A. affinis is always genetically divergent from other Alona species.

The genus Ephemeroporus is present in both Australian and New Zealand lakes (Table 1). However, the species documented in New Zealand lakes may not be correct. For example, Burns et al. (1984) reported the distribution of Ephemeroporus barroisi Richard, 1894 in a New Zealand lake (Fig. 1). E. barroisi was previously described as Pleuroxus barroisi or Chydorus barroisi (Frey 1982b). There are other closely related species described within the barroisi complex such as hybridus and tridentatus. Based on a distinct, single, large median pore in instar I, Ephemeroporus was described as different from the Chydorus genus. Some species such as tridentatus are present in Australian lakes (Frey 1982b; Shiel & Dickson 1995). A headshield of Chydorus like Cladocera has been recorded from the surface sediment sample of a lowland forested lake, L0407, from the South Island (Fig. 2b). This specimen is possibly the headshield of the species of Ephemeroporus. However, the distribution of E. barroisi in New Zealand lakes is poorly known.

Similarly, the taxonomy of Chydorus sphaericus Müller, 1776, a species regarded as cosmopolitan and present at nearly all latitudes and elevations, needs to be reconsidered for New Zealand. Until recently C. sphaericus was one of the commonly documented chydorid Cladocera in New Zealand lakes (Burns et al. 1984; Kattel & Augustinus 2010). However, Frey (1980a) argued that C. sphaericus may have two species groups, each with an unknown number of species worldwide. A comprehensive revision for sphaericus complex of Chydorus in New Zealand is required through DNA analysis.

Frey (1995) argued that chydorid Cladocera in New Zealand and Australian lakes must have evolved much later than their northern hemisphere counterparts, and the separation of Gondwana from Pangea ca 180 million years ago might have played a critical role, with the expanding oceans between them gradually creating a barrier to passive dispersal of cladoceran eggs. Consequently, the speciation of the chydorid Cladocera in the southern hemisphere has become significantly different from that of northern hemisphere taxa. For example, the chydorid genus Bryospilus (Table 1) occurs in wet forests of Puerto Rico, Venezuela, Cameroon and New Zealand (Frey 1980b). The species Bryospilus bifidus Frey, 1980 is endemic to New Zealand and recorded in Nothofagus forest litter from the South Island (Frey 1980b). Morphologically, the genus Bryospilus closely resembles the genus Monospilus (Frey 1980b). However, the unique microhabitat structure of Bryospilus today suggests that these two genera must have adapted separately over a long period of time.

Bryospilus in New Zealand lakes is particularly important for understanding the changing climates and vegetation that accompanied the cycles of glaciation during the Quaternary. Monospilus dispar Sars, 1862 is widely distributed in Europe, preferring mainly littoral sandy/muddy substrata (Kattel et al. 2006). Chiambeng & Dumont (2005) recorded M. dispar in the rain forests of Cameroon and argued that this species may have been able to survive the post-Miocene cooling and aridification in Africa. Records of M. dispar from New Zealand lakes are rare, although a headshield of a Monospilus-like genus has been recorded from the surface sediment sample from a lowland forest lake L0405 in the South Island (Fig. 2c). Whilst the taxonomy of Monospilus is yet to be established, it is important that the spatial and temporal distribution patterns of Monospilus and Bryospilus in New Zealand lakes are known so that they can provide information regarding the major climatic events and ecological shifts in the past that forced these two species to adapt separately.

Adamowicz & Sacherova (2006) hypothesized that a directional evolution of chydorid Cladocera occurred using loss or gain of morphological characters in phylogeny-based methods. They argued that both loss and gain of structures during evolution may influence the probable direction of the ecological shifts (Adamowicz & Sacherova 2006). The morphological (taxonomic) species concept considers that species may be separated by means of ecological adaptation as well as by reproductive isolation (Korovchinsky 1996). However, it appears that factors including micro-habitat structure and body character evolve together for adaptation to climates which then determine the large-scale ecological shifts in some species of chydorid Cladocera. Nevertheless, some species remain unchanged. For example, Graptoleberis testudinaria Fischer, 1848 are widely distributed in both hemispheres and have changed little in New Zealand lakes (Table 1). They commonly colonize structural habitats of aquatic macrophytes and no differences have been reported in complex morphological character and species variation (Fryer 1968).

Cladoceran such as Alonella excisa Fischer, 1854 are also widely distributed in both hemispheres and display no taxonomic confusion. Headshields of A. excisa have been recorded from surface sediment samples collected from a lowland lake, L0412, in the South Island of New Zealand (Fig. 2d). However, unlike Alonella, some other chydorid cladocerans such as Pleuroxus and Alona that are found in both hemispheres have evolved as complex groups of genera in the southern hemisphere, including New Zealand and Australia.

Pleuroxus group

The genus Pleuroxus is one of most complex genera amongst the chydorid Cladocera (Frey 1993a ,b). They have two distinct groups, aduncus and laevis. The P. aduncus group is not fully related to Pleuroxus in Australia and New Zealand as it may have several subspecies within it (Frey 1993a). Some New Zealand literature published has cited Pleuroxus aduncus Jurine, 1820 incorrectly (e.g. Green 1966). Frey (1993b) proposed sub-division of the genus Pleuroxus into Tylopleuroxus for the southern hemisphere and Picripleuroxus for the northern hemisphere. However, Smirnov et al. (2006) rejected Frey's subgeneric classification method and proposed using a genetically advanced method such as DNA markers in order to construct a consistent phylogenetic tree for this genus. Recently, surprising results have emerged from South Africa on Pleuroxus-like chydorids (Smirnov 2007) indicating that Australia and New Zealand may not be the exception in having Pleuroxus-like chydorids. Now several new subspecies within the Pleuroxus genus have been discovered in the Southern Hemisphere (Smirnov 2007). Currently, two Pleuroxus species, both belonging to aduncus complex, have been described from New Zealand lakes, namely: Pleuroxus hastirostris Sars, 1904 and Pleuroxus hevenacus Frey, 1991 (Table 1).

Alona group

One of the largest chydorid subfamilies, Aloninae, has been reviewed several times (e.g. Flösner & Frey 1970; Frey 1959 ,1987 ,1988 ,1991b; Sinev 2001 ,2004; Van Damme et al. 2010). Most species within this subfamily have been removed or given new names after investigation of their taxonomy and systematics (e.g. Sinev 2004; Van Damme et al. 2010). Alona Baird, 1843 is a large lump genus within which Aloninae from many parts of the world have been placed (Fryer 1968; Frey 1995; Korovchinsky 2006; Van Damme et al. 2010). Until recently, 14 Aloninane genera have been considered valid for taxonomic identification (Van Damme et al. 2010). Hence, the phylogenetic position of many Aloninae is yet to be resolved and the genus Alona Baird, 1843 is likely to have many endemic species within it. More importantly, the holarctic (distribution across the continents) speciation of southern hemisphere Alona has not been adequately substantiated (Frey 1982c).

Morphological investigations, as well as DNA analyses, have yet to be undertaken on individual Alona populations. For example, Sinev (2004) proposed that the previously documented species Alona macrocopa needs to be placed in a new genus, Armatalona, within the subfamily Alonanie (Table 1, Fig. 3(i)). DNA analysis of New Zealand Alona by Sacherova & Hebert (2003) suggests that the phylogeny of Alona is more complex than that of other chydorids. Furthermore, a mitochondrial study by Sacherova & Hebert (2003) on the phylogenetic history of 37 chydorid species collected from many parts of the world, including New Zealand, suggests that the existing taxonomic system is not accurate.

Fig. 3  Two members of the subfamily Aloninae. (i) Armatalona macocopa Sars, 1894 and (ii) Alona setigera Brehm, 1931 commonly present in New Zealand lakes. (i) Armatalona macrocopa Sars, 1894. A. lateral view; B. dorso lateral view; C. post abdomen; D. head pores; E. antennae II. scale bar: A–B = 0.1 mm, C–E = 0.02 mm (adopted after Sinev 2007). (ii) Alona setigera Brehm, 1931. a, b, general view of adult female; c, postabdomen female; d, headpore female; e, headshield female; f, labrum; g, h, general view of male; i, postabdomen male (adopted after Santos-Wisniewski et al. 2001).

The record of small Alona such as Alona guttata Sars, 1862 in Auckland maar lake sediments suggests that they have been present in New Zealand for at least the past 30 cal kyr BP and became dominant during the early Holocene (Kattel & Augustinus 2010). Both modern and fossil populations of Alona guttata Sars, 1862 have been recorded in regions with sub-zero temperatures such as Arctic Greenland (Frey 1991b) and the alpine Himalayas (Swar & Fernando 1979; Fernando & Kanduru 1984), mild northern and southern temperate regions of the USA (Harmsworth 1968) and New Zealand (Burger et al. 2002; Kattel & Augustinus 2010), as well as in the tropics of Brazil (Santos-Wisniewski et al. 2001). Fryer (1968) reported that, unlike other small Alona, A. guttata occurs in both large lakes and small ponds and is tolerant of a wide range of physicochemical conditions. Schallenberg et al. (2003) recorded Alona sp. (possibly a member of the small Alona group) from the Lake Waihola, a lowland shallow coastal, regularly saline-influenced lake in South Island, New Zealand, indicating an increased tolerance to salinity by these biota.

There are many similarities between the morphology of Alona guttata Sars, 1862 and another small Alona, Alona rectangula Sars, 1862 (Fryer 1968). For example, the shape and size of the carapace, head shield and the number of median pores present in these species are similar. Even within small geographic areas of Europe sub-species of Alona guttata have been reported by Kurz (Frey 1962 ,1988). Consequently, along with the other small Alona, including A. rectangula, the subspecies A. guttata (e.g. A. guttata var tuberculata Kurz, 1874) makes identification of small Alona more difficult (Frey 1960a ,b). The global distribution of small Alona requires further investigation.

The distribution of Alona rectangula Sars, 1862 has not been adequately documented from New Zealand lakes. A. rectangula has been incorrectly documented from sub-Antarctic islands, with the actual species inhabiting these islands being Alona weinecki Studer, 1878 (Frey 1988). Sacherova & Hebert (2003) argued that A. rectangula is restricted to Europe and a very similar species, Alona circumfimbriata n. sp., is restricted to North America. According to these authors, there is no evidence of A. rectangula being present in New Zealand lakes, and they suggest that there may be more sub-genera present within the genus Alona.

Some workers suggest that the small Alona recorded in New Zealand lakes could be Alona setigera Brehm, 1931 (Table 1). Brehm (1931) described A. setigera, a subspecies of A. guttata. However, unlike in A. guttata (Sinev 1999a), there are only two median pores in A. setigera and Brehm's description is incorrect (Sinev 1999a; Santos-Wisniewski et al. 2001; Fig. 3(ii)). However, the configuration of the lateral pores of A. setigera resembles that of the northern hemisphere species Alona costata Sars, 1862 or Alona rustica Scott, 1895, consisting of short transverse slits and pocket-like structures retained under the lateral pores (Flössner & Frey 1970; Sinev 1999b). Two different headshields of small Alona (Fig. 1e,f), possibly from Alona setigera Brehm, 1931, were recorded from the surface sediment samples of two South Island lakes, L0423 and L0419. However, neither of the headshields have pocket-like structures retained under the lateral pores and the shape and size of these headshields also vary significantly. An inventory of Cladocera in Australia proposed that A. guttata should come under the genus Biapertura and the species A. setigera should also be Biapertura setigera (Smirnov & Timms 1983). An extensive review of their morphology and genetic variability is required in order to verify the existence of endemic populations of chydorid Cladocera either in the form of Alona or in the form of Biapertura in New Zealand lakes.

Most chydorid Cladocera, including the small Alona group, may have adapted very well to New Zealand environments. The two small Alona, Aramatalona macrocopa and Alona setigera, were widely recognized as southern hemisphere chydorids, possibly endemic to New Zealand and Australia (Smirnov & Timms 1983; Smirnov 1989; Sinev 2007). However, both species have recently been recorded in the tropics of Thailand and Brazil (Fig. 3; Santos-Wisniewski et al. 2001; Sinev 2007). What makes small Alona Baird, 1843 (A. guttata, A. macrocopa and A. setigera) highly tolerant to a wide range of climates is not clear. However, given their adaptation to cold, hot, dry and humid climates (Harmsworth 1968; Swar & Fernando 1979; Fernando & Kanduru 1984; Frey 1991b), they appear to have been able to adapt to the glacial–interglacial cycles that dominated the Quaternary.

As the temperature of much of New Zealand during the Last Glacial Maximum (ca 18–28 cal kyr BP) was like today in the sub-Antarctic regions, it is likely that the most cold-tolerant chydorid Cladocera would have undergone a reproductive phase (Frey 1982a) during spring which may have then supported continuous and viable populations of most species of small Alona despite the harsh climate. In addition, all members of the chydoridae live in a broad range of habitats, including the littoral zone, associated with macrophytes and organic-rich sediments, sand and boulders (e.g. Fryer 1968 ,1974; Kattel et al. 2006).

The range in size and diversity of feeding behaviour of Anomopods may have played a significant role in niche separation as well as speciation over the Cenozoic (Fryer 1968 ,1995). Galaxias fish fossils discovered in a Miocene lake in Otago (Lee et al. 2007) further support the existence of lake ecosystems in New Zealand for millions of years, in which the chydorid Cladocera should have played an important bottom-up role in food web dynamics. However, the debate regarding biogeography, taxonomy and systematics of chydorid Cladocera is still unresolved.

Future prospects for New Zealand chydorid Cladocera research

New Zealand scientists face difficulties in using cladocerans to assess ecological and environmental changes in New Zealand due to poor knowledge of their taxonomy and biogeography. This is important as they are one of the significant bio-indicators of global change from lacustrine environments (Lotter et al. 1997; Battarbee 2000; Kattel & Augustinus 2010). In contrast with the situation in the northern hemisphere, study of the chydorid Cladocera is in its infancy in New Zealand. Until recently, most chydorid Cladocera recorded as both modern and fossil assemblages in New Zealand lakes were regarded as cosmopolitan species due to the use of taxonomic keys based on northern hemisphere taxa. Some members of the chydorid subfamily Aloninae, small Alona (A. guttata, A. setigera) for example, appear to be well distributed in New Zealand lakes and elsewhere. However, studies such as that by Frey (1995) suggest that following the breakup of Gondwana, the New Zealand chydorid Cladocera may have evolved differently from their northern hemisphere counterparts. Consequently a significant variability in speciation has occurred in some members of the Chydoridae.

One of the important requirements for improving the taxonomy and biogeography of chydorid Cladocera is to examine the consequences of the geological history of New Zealand on adaptation of these animals. A detailed morphological character of body parts of extant and fossil chydorid cladocerans would continue to improve taxonomy and help understanding of the biogeography and ecological adaptation of these animals in New Zealand's freshwater environments. However, taxonomic interpretation based on DNA analysis of both fossils and extant chydorid cladocerans can be the only reliable option to optimize our efforts in global environmental change research for various time scales through the use of these animals.

Acknowledgements

We would like to acknowledge two anonymous reviewers. Their constructive suggestions were significant in improving the quality of this paper. We are also grateful to Marcus Vandergoes of GNS Science for providing surface sediment samples of South Island lakes, and the School of Environment at the University of Auckland, New Zealand, for provision of laboratory facilities and assistance. This work was supported by the University of Auckland Research Fund (3608532) Award to PCA.